Biological Integrity: a Long-Neglected Aspect of Water Resource Management Author(S): James R

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Biological Integrity: A Long-Neglected Aspect of Water Resource Management Author(s): James R. Karr Source: Ecological Applications, Vol. 1, No. 1 (Feb., 1991), pp. 66-84 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1941848 . Accessed: 12/03/2014 10:41

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This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions Ecological Applications,1(1), 1991, pp. 66-84 ? 1991 by the Ecological Society of America

BIOLOGICAL INTEGRITY: A LONG-NEGLECTED ASPECT OF WATER RESOURCE MANAGEMENT1

JAMES R. KARR Departmentof Biology, Virginia Polytechnic Institute and State University, Blacksburg,Virginia 24061-0406 USA

Abstract. Waterof sufficient quality and quantity is criticalto all life.Increasing human populationand growthof technologyrequire human society to devotemore and more attentionto protectionof adequatesupplies of water.Although perception of biological degradationstimulated current state and federal legislation on thequality of water resources, thatbiological focus was lost in the searchfor easily measured physical and chemical surrogates.The "fishableand swimmable"goal of the Water Pollution Control Act of 1972 (PL 92-500)and its chargeto "restoreand maintain"biotic integrity illustrate that law's biologicalunderpinning. Further, the need foroperational definitions of termslike "biologicalintegrity" and "unreasonabledegradation" and forecologically sound tools to mea- suredivergence from societal goals have increasedinterest in biologicalmonitoring. As- sessmentof water resource quality by sampling biological communities in the field (ambient biologicalmonitoring) is a promisingapproach that requires expanded use of ecological expertise.One suchapproach, the Index of Biotic Integrity (IBI), providesa broadlybased, multiparametertool for the assessment of biotic integrity in runningwaters. IBI based on fishcommunity attributes has nowbeen applied widely in NorthAmerica. The successof IBI has stimulatedthe development of similarapproaches using other aquatic taxa. Ex- pandeduse of ecologicalexpertise in ambientbiological monitoring is essentialto the protectionof waterresources. Ecologists have theexpertise to contributesignificantly to thoseprograms. Key words: biologicalintegrity; biological monitoring; fish community; Index of Biotic Integrity (IBI); indexesof degradation; indicators; water pollution; water resources.

INTRODUCTION AccountingOffice 1987, NationalResource Council Degradationof water resources has longbeen a con- 1987,Simon et al. 1988,Davis and Simon1989, Day cernof human society. Regions with dense human pop- 1989).A GovernmentAccounting Office study (Gen- ulationswere the earliest areas at risk,but watersin eral AccountingOffice 1989) in UnitedStates Envi- isolatedareas have also experienceddegradation. The ronmentalProtection Agency (USEPA) Region 10 earliestanthropogenic threats to waterresources were (NorthwestUnited States) showed that 602 segments oftenassociated with human health, especially disease- of riversand streamsare water-qualitylimited (i.e., causing organismsand oxygen-demandingwastes limitedby chemicalcontamination). Further, a na- (Meybeckand Helmer1989). Early emphasis (e.g., the tionwideUnited States Fish and WildlifeService sur- saprobicsystem: Kolkwitz and Marsson1908, 1909) veyfound reduced fishery potential because of chem- was on controllingthese contaminants in urbanareas icalproblems in 56%ofthe stream segments with water whereeffluents exceeded the natural waste assimilation resourcedegradation (Judy et al. 1984).Of equal con- capabilitiesof waters. An industry developed to collect, cern,the study found that 49% wereimpaired by deg- treat,consolidate, and release household sewage through radationin physical habitat and 67% by flow alteration, point-sourceoutflows. The goal was to see thatthe neitherof whichare treatedby existingUSEPA pro- streams'or lakes' abilityto assimilatethose wastes grams.In 1986,USEPA acknowledgedthat nonpoint werenot exceeded, using the philosophy that "dilution sourcesaffect 65% of impairedstream miles, 76% of is thesolution to pollution."As technologyadvanced, impairedlake acres, and 45% of impaired estuary square chemicaland physicalindicators became the primary miles(General Accounting Office 1989; citing USEPA regulatorytool to protectwater resources. 1986 National WaterQuality Inventory Report to However,continuing declines in the qualityand Congress).From 1972 to 1982,four times more lake quantityof water resources despite massive regulatory acreagedeteriorated than improved in quality(John- effortscall attentionto the inadequaciesof existing son 1989).Because most water resource programs con- programs(EPA 1987, 1988a,c, 1989c, 1990,General centrateon humanhealth rather than a broaderarray of naturalresource issues, many water resource prob- lemspersist (Huber 1989). I Manuscript received 16 October 1989; revised 26 June As human populationsand theirtechnology in- 1990; accepted 27 June 1990. crease,impacts, such as thefollowing, are too diverse

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions February1991 BIOTIC INTEGRITY AND WATER RESOURCES 67 forchemical control approaches to protectthe resource kansas,Rohm et al. 1987),and biologicalcriteria in (Karrand Dudley 1981, Karr et al. 1985b):(a) pro- assessmentsand monitoring (Michael et al. 1989).Fol- ductionof domestic effluents, (b) erosionfollowing al- lowinga detailed,statewide program to evaluateam- terationof landscapes by agriculture, urbanization, and bient(field) biological monitoring, Ohio is incorporat- forestry,(c) alterationof stream channels and lake mar- ingbiological monitoring into regulations for attainment ginsthrough dams, channelization, drainage and filling ofthe goals of the Clean Water Act. An additional16 ofwetlands, and dredgingfor navigation, (d) diversion stateshave activeinterest and 23 otherstates are ex- or otherflow alteration, (e) overharvestof biological pressirnginterest in biocriteria(Marcy 1989). Some resources,and (f)proliferation oftoxic chemicals from (Colorado)retain a toxicand effluent focus while others pointand nonpointsources. Treatment of the impact (Ohio) incorporatea broader biological integrity goal. ofmultiple stresses is in itsinfancy (Preston and Bed- Theseadvances came about because of recognition that ford1988, Cairns and Niederlehner1989). Recogni- waterresource problems involve biological as wellas tionof these problems stimulated research to develop physicochemicaland socioeconomicissues. improvedapproaches for assessing the integrity oreco- Philosophicalshifts within state and federalagencies logicalhealth of waterresource systems (Karr 1981, suggestthat the short-sighted and incomplete approach Karret al. 1986,Ohio EPA 1988,Plafkin et al. 1989). to waterresources management ("making clean water Growingconcern about the need to resolvethe bio- willsolve water resource problems") can be overcome. diversitycrisis (OTA 1987) is a parallelbut broader Replacementof this approach with sophisticated, problem.For thefirst time in severaldecades, the op- quantitativeassessments based on ecologicalprinciples portunityto altersociety's approach to theprotection is morelikely to protectwater resources from the wide ofwater resources presents itself. rangeof human actions that degrade those resources. Severalfederal agencies and manystates are calling Whereasthe foundationsfor these advances have forevaluation and implementationofprograms of di- existedfor perhaps two decades three factors have con- rectbiological monitoring. New philosophiesguide tributedto rapidadvances in thelast decade:(a) the theseefforts and signalmajor shifts that will be instru- developmentof integrativeecological indexes (Karr mentalin "restoringand maintaining"biological in- 1981,Karr et al. 1986,Ohio EPA 1988,Plafkin et al. tegrityof thenation's waters, the explicit mandate of 1989),(b) thedevelopment of the ecoregion approach PL 92-500(Water Quality Act Amendments of 1972) (Hugheset al. 1986,1987, Omernik 1987, Hughes and and amendments.USEPA has calledfor the following: Larsen1988), and (c) recognitionof the importance of (a) inclusionof biologicalcriteria in its water-qualitycumulative impact assessment at regionalscales (Pres- standardsprogram (EPA 1988a), (b) restructuringof ton and Bedford1988). The challengefor basic and existingmonitoring programs to documentthe impact appliedecologists in thenext decade will be to ensure of regulatoryprograms (EPA 1989a), (c) evaluation thatecological principles are used to improvethe na- and controlof nonpointpollution (EPA 1989b),(d) tion'sprograms to protect and manage water resources. coordinationof chemical sampling with biological sur- Anotherbenefit will be theopportunity to conductad- veys(EPA 1984),(e) ecologicalrisk assessment (EPA ditionalecological research. 1988b),(f) theincorporation of "good science"at all Here,I describeimpediments to an integrativeeco- levelsof waterresource policy (EPA 1988c, 1989b), logicalapproach to protectionof water resources, de- and (g) adoptionof narrativebiological criteria into scribea recentlydeveloped approach for assessment statewater-quality standards during the FY 1991-1993 ofbiologicalintegrity ofa waterresource, and speculate triennium(EPA 1990).(Biological criteria [Biocriteria] on the futureof biologyin the protectionof water is a code wordfor "indicator of ecological conditions" resources. or "biologicalintegrity compared to some least dis- turbedreference community.") EPA (1988a) and oth- WHYHAS IT TAKENSo LONG? ers(Van Putten1989) call fordevelopment of biolog- Althoughdegradation in the abilityof waterre- ical criteriato protectterrestrial wildlife from the sourcesto supportbiological activity was thefirst sign negativeeffects of human activities on waterresources. ofa problem,society embraced approaches to improve UnitedStates Geological Survey (Hirsch et al. 1988) waterquality that were dominantly not biological. Rea- andTennessee Valley Authority (Saylor and Scott 1987) sonsfor limited use ofintegrative biological approach- are expandingtheir use of biologicalmonitoring as es to protectwater resources are complex.I identified well. thefollowing eight factors. Moststates are expandingtheir biological monitor- Dominanceof reductionistviewpoints. -The domi- ing programs(Simon et al. 1988, Davis and Simon nantreductionist views of several disciplines involved 1989, KilkellyEnvironmental Associates 1989), al- in stateand federalwater management have been, and thoughthe approaches differ among states. Some have remain,a majorimpediment. First, few knowledgeable adoptedlegal biologicalcriteria (Florida, Vermont), ecologistsare willingto eitherhelp developand im- biological-baseduse designations (e.g., excellent warm- plementcriteria and standardsor challengethe con- waterhabitat: Maine, Courtemanchet al. 1989; Ar- ceptualunderpinnings of suchapproaches. Standards

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 68 JAMES R. KARR Ecological Applications Vol. 1,No. 1 arethe legally established rules consisting of two parts, constraintson the use of biologyin protectionof water designateduses and criteria.Designated uses are the resources.The firstwater-quality act was probablythe purposesor benefitsto be derivedfrom a waterbody Refuse Act of 1899 createdto treatthe growingprob- (e.g.,aquatic life, irrigation water, and drinkingwater), lem of disease and oil pollution of navigable waters. and criteriaare the conditions presumed to supportor Since the 1940s a seriesof laws and amendmentswere protectthe designateduses. Dissolved oxygen(DO) passed underthe generalrubric, Water Pollution Con- maynot fall below 5 mg/L,for example, if the desig- trolAct (WPCA; also WaterQuality Act or Clean Wa- nateduse is a coldwaterfishery. Second, engineers often ter Act). Amendments passed in 1948, 1956, 1961, failto incorporate concern for biotic impairment. Third, 1965, 1966, and 1970 established several trends:(1) politiciansimplement programs based on local inter- more money for constructionand technologydevel- ests and shorttime scales. Finally,planners attack opment,(2) expanded lists of pollutantsfor treatment, problemsas if ecosystemdysfunctions could be re- and (3) increasesin enforcementefforts to controlpoint versedwithout broad understanding ofthe whole sys- sources of pollution. These effortssuccessfully con- tem.Overall, a lack of interdisciplinarybreadth, and trolleddisease and, secondarily,reduced dischargeof especiallya lack of groundingin biologicaltheory, suspended solids (especially particulate organic car- hampersdevelopment of sound water resource policy. bon) that produced high biological oxygen demand A specialneed existsto accountfor actual behavior (BOD) near wastewatertreatment outflows. The grow- and variabilityof populations, communities, and eco- ing array of chemicals from industrialplants, urban systemsthrough adequate understanding of historical runoff,and agriculturalsediments, nutrients, and pes- and currentbehavior (Schindler 1987). ticides were inadequatelytreated. Limitedlegal and regulatoryprograms. -Water law The burdenof proofin documentingecosystem deg- withinthe American legal system is a complexinte- radation and establishingcausal links to specificdis- grationof federal and stateconstitutions (fundamental chargesfell on thegovernment (Ward and Loftis1989). law), statutesand ordinances(acts at stateor federal However, establishingthe cause of degradationwas and local levels),administrative regulations (formu- difficultand enforcementactions were rarelysuccess- latedand implementedby agencies),executive orders ful. First,no rigorouslydefined water-quality criteria (ordersby state and federalchief executives), and com- were available. Second, fewtools existedto accurately monlaw courtdecisions (Goldfarb 1988). and effectivelyportray the results of regulatorypro- As a result,responsibility for regulation, protection, grams. and developmentof waterresources is vestedin a By 1972, Congress recognizedthe need to revamp patchworkof local, state,national, and internationalwater resource programs. The WPCA Amendmentsof agencies.Although protection of water resources is the 1972 (PL 92-500), which came on the heels of the first primarygoal ofwater law, the law is notadequate to "Earth Day" and heightenedenvironmental awareness protectwater resources. For example, current water law at the national level in the 1960s, containedfar-reach- evolvedbefore relationships between ground and sur- ing provisions, including strongerenforcement, in- facewater were understood. This issuehighlights the creased federal involvement in water resource pro- fundamentallydifferent approaches used in legaland grams,and strictdeadlines to end pollution by 1985. scientificcircumstances. Historically, courts could only These were to be implementedprimarily by achieving imposeeffluent controls with proof, based on a pre- technology-based limits for point-source effluents ponderanceof evidence, that an effluentwas degrading (Levin and Kimball 1984, Ward and Loftis 1989). For a waterresource. Science is moreconcerned with risk the firsttime, water quality standards covered intra- managementthat involves evaluation of probabilities state and interstatewaters. Two visionaryphrases in ofdamage. theact dealt witha "fishableand swimmablegoal" and Anothercommon but technicallyindefensible di- thecharge to "restoreand maintainthe physical, chem- chotomythat is firmlyingrained in waterlaw is sep- ical, and biological integrityof the Nation's waters." aratelegal frameworks for water quality and quantity These phrases explicitlycall attentionto the need to (McDonnell1990). For example, water rights law dom- permit". . . all formsof natural aquatic life (the ulti- inatesin the southwest where water supplies are limited mate goal of water quality management)" (Meybeck (6% ofUnited States supply but 31% ofuse), and water and Helmer 1989). qualityissues dominate in the east where water supplies Although the new emphasis on technology-based generallyexceed demand (37% of supplyand 8% of controlswas heralded as revolutionary,implementa- use; Anonymous1990). Toxicological(water quality) tion programswere usually limited to establishment approachesdominate efforts to protectbiological com- of effluentlimitations, an improved dischargepermit ponentsof waterresources in theeast while methods system(National PollutantDischarge Elimination Sys- to protectin-stream flows (water quantity) dominate tem [NPDES]), performancestandards for new plants in thewest (Bain and Boltz 1989). and industries,and the call forsewer and waste treat- Theevolution of federal water quality legislation (and ment plants in all municipalitiesin the United States. the regulationsthat supportit) illustrateadditional Regulationscontinued to stressrules and standardsfor

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions February1991 BIOTIC INTEGRITY AND WATER RESOURCES 69 effluentsrather than measuring the biological effects in phasis fromtechnology-based controls with simple thereceiving water body, because regulators feared a chemicalwater-quality standards to protectionof spe- returnto the 1960s "burdenof proof' days. (Recall cificwater bodies (Plafkin 1989). thelaw vs. sciencedichotomy mentioned previously.) The 1980s have seen a major shiftin philosophy Thus,the focus on chemicalparameters continued, or, withrecognition of the inadequacy of earlier approach- whena biologicalperspective was used,the emphasis es as outlinedin a reportentitled "Surface Water Mon- was on acuteand laterchronic effects of chemical pol- itoring:A Frameworkfor Change" (EPA 1987).At last, lutantson laboratoryorganisms. Many have expressed ambientmonitoring of biological integrity is being rec- disappointmentthat the visionary law was usedso in- ognizedas a direct,comprehensive indicator of eco- adequately(Anonymous 198 la, b, 1983). logicalconditions and, thus, the quality of a waterre- Althoughthe call forprotection of bioticintegrity source. Although some arguethat "the waterquality was explicitin the 1972 amendments,point-source criteria approach has servedthe science and theneeds effluentsremained the primary target of regulatory ef- of societywell" (Kimerle1986), continuing degrada- fortsfor at leastthree reasons: (a) biologicalintegrity tion of waterresources stimulated evolution in three was onlyone of several aspects explicitly protected, (b) areasof USEPA policy:(1) effortsto documentenvi- politicallyand logisticallypoint sources were easier to ronmentalvariability across landscapes and thusde- cleanup, and (c) numericalpollution standards were velop appropriateregional adjustments of standards thoughtto be bothlegally defensible and sufficientto (EPA 1983),(2) effortsto developand implementap- protectwater resources. proachesfor the direct assessment of bioticintegrity Successwith the effluent-control approach on point (Karret al. 1986,Plafkin et al. 1989),and (3) recog- sourcesof pollution made the effects of nonpoint-source nition of the need to assess and mitigatecumulative (NPS) problemsmore obvious. However, programs to impactsof human society (Karr and Dudley 1981, Karr controlNPS pollutionwere (and remain today) largely 1987,Bedford and Preston1988, Preston and Bedford unsuccessfulbecause of difficulties involved in apply- 1988, EPA 1988b). ingpoint-source approaches to diffuse nonpoint-source Definitionof biologicalintegrity. -USEPA con- problems(Karr 1990) and because of our unwillingness vened a symposium(Ballentine and Guarraia1975) on as a societyto limitprivate land rightsfor the public theintegrity of water soon after passage of PL 92-500, good. Thompson(1989) providesa comprehensive,but no cleardefinition ofbiotic integrity emerged. Many chemicallyoriented analysis of the continuingprob- authorsadvocated use of a holisticperspective. Karr lemsof NPS pollution. and Dudley(1981) arguedthat the "integrity" objec- The nextmajor legislative action came in 1977with tive encompassesall factorsaffecting the ecosystem passageof the Clean WaterAct (CWA). As a result, and developeda now widelyquoted definition of bi- emphasisshifted from conventional pollutants (e.g., ologicalintegrity as the ability to supportand maintain fecalcoliform and BOD) to thegrowing list of toxic "a balanced,integrated, adaptive community of or- chemicalsreleased into the nation's waters. Although ganismshaving a speciescomposition, diversity, and a widerperspective appeared in the 1972 and 1977 functionalorganization comparable to thatof natural legislation(e.g., "fishable," "swimmable," and "biotic habitatof the region." integrity"),the primaryregulatory approach of both A morerecent paper defined ecological health (an EPA and thestates focused on technology-basedcon- umbrellagoal, the maintenanceof whichmotivates trolsto limitpoint-source pollutants discharged into virtuallyall environmentallegislation) as follows:"a bodiesof water.All too frequentlyefforts to measure biological system... can be consideredhealthy when progresstoward water-quality goals used administra- itsinherent potential is realized,its condition is stable, tive accounting(counts of permitsissued or point itscapacity for self-repair when perturbed is preserved, sourcesregulated) rather than assessment of environ- andminimal external support for management is need- mentalresults. An inabilityto associatewater-quality ed" (Karret al. 1986). based standardswith biological integrity also limited While thesedefinitions establish broad biological thesuccess of effortsto protectwater resources, espe- goals to replacethe morenarrowly defined chemical ciallyin viewof the combined (synergistic, antagonis- criteria,their use dependsupon developmentof biotic,and additive: Risser 1988) effects of numerous pol- logicalcriteria based on ecologicalprinciples. Unfor- lutantsand other human impacts (cumulative impacts: tunately,most theoretically oriented ecologists have Prestonand Bedford1988). Althoughchemical and beenreluctant to participatein theapplication of their physicalapproaches are legally defensible (Mount 1985), knowledgeto appliedproblems (Schindler 1987), and theycannot measure complex attributes such as eco- a cynicalattitude about the utility of ecologistsdom- logicalhealth or "bioticintegrity." inatesin some quarters(Wilk 1985, Kareiva 1990). Becauseof widespread public support, the Congress Widespreaduse of single-speciesbioassays, compli- passed the WaterQuality Act of 1987, overridinga catedmodels, and impact-statement studies have been presidentialveto. When combined with regulations de- singularlyunsuccessful at predictingthe effects of an- velopedin 1983 and 1985,this act changedthe em- thropogenicstress on biologicalsystems (Schindler

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 70 JAMES R. KARR EcologicalApplications Vol. 1,No. 1 1987). Studiesof populationdynamics, food-web or- indexesand could be used to detectdegradation and ganization,and taxonomicstructure of communities identifyits cause and to determineif improvement re- have been moresuccessful (Schindler 1987). sultsfrom management actions. In thebest ofall worlds Besidesdefining biological integrity, success at in- thesecould be used in a regulatorycontext to prevent corporatingbiotic integrity into water resource man- degradationand thuspreserve high quality water re- agementdepends on an appropriate,cost-effective pro- sourcesystems. Indicators for general usage must be cedureto measurebiotic impairment. The indexof applicablein a widerange of waterresource systems bioticintegrity (described in How to measurebiotic and be successful"in measuringattainment of the bi- integrity,below) provides one suchapproach. ologicalintegrity goals of the Clean Water Act" (Ohio Indexesto assessbiological integrity. -Early efforts EPA 1988). todevelop biological indexes concentrated on detecting Region-basedquantitative definitions of ecological a narrowrange of variation in biological integrity (Taub health.-The idea of chemical-specifictoxicological 1987,Ford 1989,Fausch et al. 1990),yielded indexes criteriaand water-qualitystandards involves defining sensitiveto onlya fewtypes of degradation(reduced contaminantlevels above whichnegative effects on DO, selectedtoxins, etc.), or providedonly a binary waterresources can be expected(Levin et al. 1989). (degraded/notdegraded) evaluation. Some evaluated But,standardized values forchemical criteria fail to fecalcontamination (Geldreich 1970) while others fo- recognizenatural geographic variation in waterchem- cused on effectsof chemicalstress on organismsat istry.Natural heavy metal concentrations in western populationor community levels (Ford 1989). Although riversare oftenwell above EPA standardslevels and valuablefor measurement of selectedanthropogenic dissolved oxygen levels often fall below standards es- effects,they were less usefulfor screening all typesof tablishedin water-qualityregulations. Many recent ef- degradation,including complex cumulative impacts. fortsto developbiological criteria call fordefinition of The saprobinsystem developed in Europe(Sladacek regional(Fausch et al. 1984,Hughes et al. 1986,Gal- 1973) focuseson biologicaloxygen demand (BOD). lant et al. 1989) and streamsize expectations(Karr Use of selectedintolerant species may reflect changes 1981,Ohio EPA 1988,Plaflin et al. 1989). such as highlevels of oxygen-demandingwastes or Manystates have adoptedOmernik's (1987) ecore- sedimentationresulting from soil erosion.Even more gion conceptas a frameworkfor refining biological complexcommunity-based indexes like the Hilsenhoff expectations(Gallant et al. 1989).Ecoregions are geo- indexfor benthic macroinvertebrates (Hilsenhoff 1982, graphicareas withinwhich stream communities are 1987)are primarily sensitive to domestic effluents. Co- relativelyhomogeneous. However, their boundaries liformcounts can identifyinputs of untreated sewage, shouldnot be flatlyaccepted because other boundaries, althoughcontamination from wildlife and livestock includingriver basins and physiographicprovinces, mayalso affect bacterial counts (Dudley and Karr 1979). maybe important.Recognition of the existence of nat- Finally,many existing biological indexes may only ap- uralgeographic variation in theecological features of plyto a narrowgeographical area (e.g., lake trout stocks undisturbedaquatic systems is essential,a realitythat in LaurentianGreat Lakes). Suchapproaches are ap- has been overlookedfor several decades in effortsto propriatewhen specific narrow impacts are knownto setrigid nationwide chemical and physicalstandards. be present,but protectionof waterresources from a Standardizationof field methods. -Standardization broadrange of humanimpacts requires a morecom- ofmethods (quality control/quality assurance [QC/QA]) prehensiveapproach. is a fundamentalprerequisite for any monitoring pro- One successfultactic of the past decade is tocombine gram.Without these, the utility of environmental mon- two or morebiological metrics into a singleindex. itoringdata can and willbe challenged(Plafkin et al. Comparisonsto assessmentof humanhealth (using 1989).The firststep is definitionof standards for sam- metricssuch as blood pressure,urine analysis, white plingecosystems or lowerlevels of biologicalorgani- bloodcell count, and temperature), orseveral econom- zation.Karr et al. (1986),Ohio EPA (1988),and Plaf- ic indicatorsare appropriate. Each metricprovides in- kinet al. (1989) provideexamples of efforts to define formationabout the sampling site and eventhe region acceptablemethods for sampling biological commu- (Steedman1988). When combined, these metrics char- nitiesin the field with minimal sampling effort. Finally, acterizethe biotic integrity in muchthe same way that theyalso attemptto formalizeanalytic procedures. a batteryof medicaltests are indicatorsof individual Linkingfieldmeasurements to enforceablemanage- health.However, it is importantto note thatgood mentoptions. -As notedabove, the 1965 Federal Wa- health,human, economic, or ecosystem, is nota simple terQuality Control Act (PL 89-234) provideda na- functionof those metrics (Karr et al. 1986). tionalframework for water-quality management. That The ideal indexwould be sensitiveto all stresses frameworkconsidered water-quality management to placedon biologicalsystems by humansociety while be a taskrequiring policies and goals (standards) against also havinglimited sensitivity to naturalvariation in whichin-stream water-quality conditions would be physicaland biologicalenvironments. An arrayof in- evaluated(Ward and Loftis1989). Problemsdevel- dicatorswould be combinedinto one or moresimple oped whenit was recognizedthat knowledge of the

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions February1991 BIOTIC INTEGRITY AND WATER RESOURCES 71 connectionsbetween in-stream conditions and theac- shouldnot be discountedon costcriteria. Further, action of dischargerswas inadequate.Operating under countingmust go beyondthe cost of data collection theassumption that point-source discharges were caus- and analysisto includecosts of building and operating ingproblems, the 1972 Act shifted from in-stream con- potentiallyunnecessary or poorlydesigned treatment ditionsto effluent conditions. Enforcement actions were plantsand costsof bad managementdecisions. Karr basedon dischargepermits whose limits were exceed- et al. (1985a) providean exampleof implementation ed. By theearly 1980s, many recognized that ignoring of tertiarydenitrification that probably yielded little in-streamconditions (Ward and Loftis1989), espe- benefitto the water resource. The mandatein the Clean ciallytheir biological context (Karr and Dudley198 1, WaterAct of 1987to reduceemphasis on construction Karret al. 1983),resulted in continueddegradation of suggestsmore widespread recognition of this issue. waterresources. Although credit is appropriatefor im- Whileprogress toward reducing the effects of these provedwater quality in some areas due to discharge eightconstraints varies, all have nowbeen widely rec- limitationsthrough permits, money was sometimes ognizedand considerableenergy is beingexpended to usedto providewastewater treatment that did notim- overcomethem. provein-stream conditions (Karr et al. 1985a, Mey- beckand Helmer 1989). Simply put, the shift to effluent How To MEASUREBIoTIC INTEGRiTY monitoringwas a high-costprogram that failed to pro- Humanactivities may alter the physical, chemical, tectthe qualityof manykey water resources due to orbiological processes associated with water resources continuingimpacts from unregulated sources (e.g., and thusmodify the residentbiological community. nonpointsources). Biologicalcriteria are valuablefor assessing these al- Mount reflectsone extremeview on thisissue (1985) terationsbecause they "directly measure the condition whenhe contendsthat the best defense for dependence oftheresource at risk, detect problems that other meth- on testingthat is based on toxicity(effluent) is thatit ods maymiss or underestimate, and providea system- is decisive;that is, toxicity-based criteria provide clear aticprocess for measuring progress resulting from the standardsfor establishing water-quality impacts. How- implementationof water quality programs"(EPA ever,decisiveness does notovercome their many de- 1990).They do notreplace chemical and toxicological ficiencieswhen one has ecologicalgoals (endpoints) in methods,but they do increasethe probability that an mind.Most chemical standards have no meaningout- assessmentprogram will detect degradation due to an- sidethe legal/regulatory context, and theyonly protect thropogenicinfluences. values includedin thestan- environmental explicitly Duringthe past decade five primary sets of variables In addition,toxicity-based cri- dard-settingprocess. havebeen identified that, when affected by human ac- teriaare not adequate as earlywarning devices for tivities,result in ecosystemdegradation (Fig. 1). Many detectionof degradation.Finally, poorly understood individualstudies demonstrate correlations (ifnot cause but importantbiological mechanisms and effectsare and effect)between degradation and some biological notincorporated into the standard-setting process (Su- indicator(e.g., species richness, changing abundance ter1990). Single-species toxicity testing may in selected of an indicatorspecies, production/respiration ratio; situationsbe wellinformed and decisive,but in many see Taub 1987,Ford 1989 forrecent reviews). How- circumstancesits decisiveness may be misleadingand ever,few attempts have been made to integrateseveral evendangerous for the resource. ofthose indicators into a singleindex. I developedsuch In short,for nearly two decades a narrowperspective an index,the index of biotic integrity (IBI) usinga set on was imposedthat was presumedto be standards of attributesthat measure organization and structure effectivebecause it was decisive, legally defensible, and offish communities. enforceablein a regulatorycontext. While I wouldnot argueagainst this approach to control point-source discharges,I wouldalso saythat sole dependenceon the The indexof biotic integrity (IBI) approachcripples society's ability to detect,much less The indexof biotic integrity was conceivedto pro- reverse,degradation due to nonpointsources of pol- vide a broadlybased and ecologicallysound tool to lution,habitat destruction, modification of flow,and evaluatebiological conditions in streams(Karr 1981). changesin theenergy base ofthe stream biota. IBI incorporatesmany attributes of fishcommunities Needforcost-effective approaches to biologicalmon- to evaluatehuman effects on a streamand its water- itoring.-Water resourcemanagers -have long argued shed. Those attributescover the rangeof ecological thatthe costs of ambient biological monitoring are too levelsfrom the individual through population, com- high(Loftis et al. 1983,EPA 1985).However, a recent munity,and ecosystem.Although initially developed compilationby Ohio EPA (Table 1) showsthat bio- foruse withfish communities, the ecological founda- logicalmonitoring may not be prohibitivelyexpensive tionof IBI can be used to developanalogous indexes comparedwith more conventionalapproaches. Al- thatapply to othertaxa, or evento combinetaxa into thoughcosts may varyamong agencies and circum- a morecomprehensive assessment of biotic integrity. stances,Table 1 demonstratesthat biotic monitoring Calculationof a fishIBI fora streamreach requires

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 72 JAMES R. KARR EcologicalApplications Vol. 1, No. 1 TABLE 1. Comparative cost analysis forsample collection,processing, and analysis forevaluation of the quality of a water resource.Data fromOhio EPA, provided by C. 0. Yoder (1989b).

Per sample* Per evaluationt Chemical/physicalwater quality 4 samples/site $1436 $ 8616 6 samples/site $2154 $12924 Bioassay Screening(acute-48-h exposure) $1191 $ 3573 Definitive(LC50: and EC50?-48 and 96 h) $1848 $ 5544 7-d (acute and chroniceffects-7-d exposure singlesample) $3052 $ 9156 7-d (as above but with composite sample collected daily) $6106 $18318 Macroinvertebratecommunityll $ 824 $ 4120 Fish communityl $ 740 $ 3700 Fish and macroinvertebrates(combined) $1564 $ 7820 * The cost to sample one location or one effluent;standard evaluation protocolsspecify multiple samples per location. t The cost to evaluate the impact of an entity;this example assumes samplingfive stream sites and one effluentdischarge. : Dose of toxicantthat is lethal (fatal) to 50% of the organismsin the testconditions at a specifiedtime. ? Concentrationat which a specifiedeffect is observed in 50% of organismstested; e.g., hemorrhaging,dilation of pupils, stop swimming. 11Using InvertebrateCommunity Index (ICI) (see textand Table 4). 1 Using Index of Biotic Integrity(IBI) (see textand Table 2). a singlesample that represents fish species composition pectedrichness from a similarundisturbed site (or, and relativeabundances. (See Karret al. 1986,Ohio regionally,least disturbed site). For theMidwest, IBI EPA 1988,and Plafkin et al. 1989for detailed sampling includesfive species richness metrics (Table 2); these and data-handlingprotocols.) Application of IBI re- includethree taxon-specific (Catostomidae [suckers], quirescareful standardization of proceduresas noted Etheostomatinaeof Percidae[darters], and Centrar- above (Whyhas it takenso long?Standardization of chidae[sunfish]), one assessingthe presence of species fieldmethods). intolerantof human activities, and one assessingtotal An additionalinnovation of IBI is thatthe value for speciesrichness (excluding exotics). The threetaxa are each metricis based on comparisonto a regionalref- selectedto representgroups that consume benthic in- erencesite with little or no influencefrom human so- vertebrates(suckers and darters)or driftingand ter- ciety(Fausch et al. 1984). Expectedvalues are based restrialinvertebrates (sunfish) as theirprimary food. on thatreference site(s) with observed values compared Assessmentsusing these taxa confirm by their presence to expectedvalues. For each metric,an indexscore of (or not)whether requisite spawning habitat and food 5 is assignedif the study site deviates only slightly from are available.Other taxa withsimilar ecological at- thereference site, 3 ifit deviatesmoderately, and 1 if tributesshould be substitutedin regionswhere these it deviatesstrongly from the undisturbedcondition. familiesare notabundant (see How to measure biotic Theseassessments require experienced biologists to set integrity:Adaptability of IBI, below and Table 2 for standardsbased on knowledgeof the regionalbiota modificationof IBI metricsin regionsoutside the Mid- (e.g.,higher species richness expected in Tennessee than west).The intolerant-speciesmetric uses the common inNebraska) and the size of stream sampled (e.g., high- observationthat within a regiona fewspecies in most er speciesrichness in largethan small streams). Thus, regionsare especiallysensitive (intolerant) to human assessmentof bioticintegrity explicitly incorporates disturbance.Intolerance to siltationis common,but biogeographicvariation into evaluation of biological othertypes of intolerancemay also be present.The systems. intolerantclass shouldbe restrictedto the 5-10% of Twelveattributes (Table 2) ofa fishcommunity are speciesthat are mostsusceptible to degradation,and rated.The sum of thoseratings (5, 3, or 1) provides shouldnot be takenas equivalentto rareand endan- an IBI value,an integrativeand quantitativeassess- gered(Karr et al. 1986). The fifthspecies richness/ mentof local biologicalintegrity (Table 3). IBI uses compositionmetric is thetotal species richness of the threegroups of metrics:species richness and compo- community.The sixthmetric in thisgroup relates to sition,trophic composition, and fishabundance and speciescomposition. Green sunfish (Lepomis cyanel- condition. lus) increasein abundancein degradedstreams of the Speciesrichness and compositionmetrics. -The first Midwest,reflecting the extentto whichdisturbance groupof six metricsevaluates the extent to whichthe permitsa speciesto dominatethe community. Other samplearea supportsreduced species richness and al- speciesused in thismetric in otherregions included teredspecies composition. Because richness varies as commoncarp (Cyprinus carpio), whitesucker (Catas- a functionof region, stream size, elevation, and stream tomuscommersonii), and gardon (Rutilus rutilus) (Mil- gradient,all sitesmust be evaluatedagainst the ex- leret al. 1988,Oberdorif and Hughes,in press).

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1. food(energy) source * type,amount, and particle size of * decreasedcoarse particulate organic matter organicmaterial entering a stream * increasedfine particulate organic matter fromthe riparian zone versus * increasedalgal production primaryproduction inthe stream * seasonalpattern ofavailable energy

2. waterquality *temperature * expandedtemperature extremes * turbidity * increasedturbidity * dissolvedoxygen * altereddiurnal cycle of dissolved oxygen * nutrients(primarily nitrogen and * increasednutrients (especially soluble ecologica phosphorus) nitrogenand phosphorus) ecological * organicand inorganic chemicals, * increasedsuspended solids impactof naturaland synthetic * increasedtoxics human-induced * heavymetals and toxic substances * alteredsalinity alterations * pH 3. habitatstructure * substratetype * decreasedstability ofsubstrate and banks *water depth and current velocity - dueto erosion and sedimentation *spawning, nursery, and hiding * moreuniform water depth places * reducedhabitat heterogeneity *diversity (pools, riffles, woody * decreasedchannel sinuosity debris) * reducedhabitat areas due to shortened *basin size and shape channel * decreasedinstream cover and riparian vegetation 4. flowregime * watervolume * alteredflow extremes (both magnitude and . temporaldistribution offloods and N frequencyofhigh and low flows) lowflows * increasedmaximum flow velocity * decreasedminimum flowvelocity * reduceddiversity ofmicrohabitat velocities *fewer protected sites

5. bioticinteractions *competition * increasedfrequency ofdiseased fish *predation * alteredprimary and secondary production *disease / . alteredtrophic structure *parasitism * altereddecomposition rates and timing * disruptionofseasonal rhythms * shiftsinspecies composition andrelative abundances * shiftsininvertebrate functional groups (increasedscrapers and decreased shredders) * shiftsintrophic guilds (increased omnivores anddecreased piscivores) * increasedfrequency offish hybridization . increasedfrequency ofexotic species

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 74 JAMESR. KARR Ecological Applications Vol. 1, No. 1 TABLE 2. Metrics used to assess biological integrityof fishcommunities based on Index of Biotic Integrity(IBI) (afterKarr 1981, Karr et al. 1986). Ratings of 5, 3, and 1 are assigned to each metricaccording to whetherits value approximates, deviates somewhat from,or deviates stronglyfrom the value expected at a comparable site that is relativelyundisturbed.

Rating of metric* Metrics 5 3 1 Species richnessand composition 1. Total numberof fishspecies* (native fishspecies)t 2. Number and identityof darterspecies (benthicspecies) Expectationsfor metrics 1- 3. Number and identityof sunfishspecies (water-columnspecies) 5 vary with streamsize 4. Number and identityof suckerspecies (long-livedspecies) and region. 5. Number and identityof intolerantspecies 6. Percentageof individuals as greensunfish (tolerant species) <5 5-20 >20 Trophic composition 7. Percentageof individuals as omnivores <20 20-45 >45 8. Percentageof individuals as insectivorouscyprinids (insectivores) >45 45-20 <20 9. Percentageof individuals as piscivores(top carnivores) > 5 5-1 < 1 Fish abundance and condition 10. Number of individuals in sample Expectationsfor metric 10 varywith streamsize and otherfactors. 11. Percentageof individuals as hybrids(exotics, or simple lithophils) 0 >0-1 > 1 12. Percentageof individuals with disease, tumors,fin damage, and skeletalanomalies 0-2 >2-5 >5 * Original IBI metricsfor midwest United States. t Generalized IBI metrics(see Miller et al. 1988).

Becauseexpectations for the species richness metrics approximatesthe upper limit of species richness (Fausch varywith stream size, we formalizeda methodto es- et al. 1984,Karr et al. 1986,Ohio EPA 1988). tablishthose expectations. A "maximumspecies rich- Trophiccomposition metrics. -This groupof three nessline" is determinedwith a plotof number of spe- metricsevaluates the trophic composition of thefish cies on streamsize (order,watershed area, or flow).A communityto assessthe energy base and trophicdy- plot of data froma watershed(Fig. 2) or ecoregion namicsof the residentbiota. All organismsrequire yieldsa distinctright triangle, the hypotenuse of which reliablesources of energy and majorefforts have been

TABLE 3. TotalIndex of Biological Integrity (IBI) scores,integrity classes, and theattributes of those classes (modified from Karr1981).

Total IBI score (sumof the 12 Integrity metric classof ratings)* site Attributes 58-60 Excellent Comparableto thebest situations without human disturbance; all regionallyexpected species for thehabitat and streamsize, including the most intolerant forms, are present with a fullarray of age (size) classes;balanced trophic structure. 48-52 Good Speciesrichness somewhat below expectation, especially due to the loss of the most intolerant forms; somespecies are present with less than optimal abundances or size distributions;trophic structure showssome signs of stress. 40-44 Fair Signsof additional deterioration include loss of intolerant forms, fewer species, highly skewed trophic structure(e.g., increasing frequency of omnivores and greensunfish or othertolerant species); older age classesof top predators may be rare. 28-34 Poor Dominatedby omnivores, tolerant forms, and habitatgeneralists; few top carnivores; growth rates and conditionfactors commonly depressed; hybrids and diseasedfish often present. 12-22 Verypoor Few fishpresent, mostly introduced or tolerantforms; hybrids common; disease, parasites, fin damage,and otheranomalies regular. t No fish Repeatedsampling finds no fish. * Siteswith values betweenclasses assigned to appropriateintegrity class followingcareful consideration of individual criteria/metricsbyinformed biologists. t No scorecan be calculatedwhere no fishwere found.

FIG. 1. Five majorclasses of environmental factors that affect aquatic biota (Karr et al. 1983).Arrows indicate the kinds ofeffects that can be expectedfrom human activities (modified from Karr et al. 1986).

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0 Range of Biotic Integrity maximumspecies 0 o 30 richnessline Very -- Excellent poor

. 20 0 0 o-cDE 105???? 00O No. Species 4- ~~~~~8D3 Darters .0~~~~~~~~~ Sunfishes

1 4 5 6 Suckers g Stream Order 7 FIG. 2. Totalnumber of fishspecies vs. streamorder for Intolerants 72 "leastdisturbed" sites along the Embarras River, Illinois. The area belowthe line of maximumspecies richness is tri- % GreenSunfish sectedand usedto rateIBI metric1, total number of species. Ratings(5, 3, 1) indicatewhether species richness at a given siteon a streamof givenorder approximates, is somewhat % Omnivores lessthan, or is farless than the species richness expected from an "excellent"fish community in theregion (modified from % Insectivorous WI//,"M////////// Fauschet al. 1984by Karr et al. 1986).Stream order is a way Cyprinids ofmeasuring stream size. % Piscivores madeto measurethe many dimensions ofproductivity. No. Fish Inds. 11////////////// Directmeasurement of productivity is costly and time consuming,especially if attemptedat severaltrophic % Hybrids levels,and theinterpretation ofresults may be ambig- uous,or evenmisleading (Schindler 1987). Thus, sev- % Diseased eralmetrics that measure divergence from expectation FIG. 3. Rangeof primary sensitivity (shaded area) for each weredeveloped as a wayto assessenergy flow through metric(see Table 2) in the Index of BioticIntegrity (from thecommunity (trophic structure). The proportionof Angermeierand Karr1986). omnivoresincreases and theproportion of insectivorouscyprinids and topcarnivores decreases in degraded systems.In all threecases theproportion of indi- Eachmetric reflects the quality of components of the vidualsin thesample is usedto ratestream reaches for fishcommunity that respond to variationin different each of thesemetrics. Scoring criteria for these func- aspectsof theaquatic system. The relativesensitivity tional metricshave been remarkablyconsistent ofthemetrics varies from region to region (Angermeier throughoutNorth America, suggesting a general pat- and Karr 1986,Karr et al. 1986,Steedman 1988), in ternfor stream fishes. partbecause metrics are differentially sensitive to var- Fish abundanceand conditionmetrics. -The last ious perturbations(siltation, flow alteration, toxins). groupof threemetrics evaluates population density In addition,natural variation in conditionsamong wa- and fishcondition. The totalnumber of individuals in tershedsreduces the probability that indexes based on the sampleis an importantparameter for evaluation one or a fewmetrics will provide reliable assessments becausedisturbed areas often have reducedfish abun- overa widegeographic area. The totalnumber of fishes dances.This metricmust be based on catchper unit decreased,and trophicstructure of the community samplingeffort, such as numberper area sampledor shifted,in areas exposedto municipaleffluent in one perunit sampling time. The finaltwo metrics evaluate study(Karr et al. 1985a). Sedimentationand other thefrequency of hybridization,apparently a function habitatalteration reduced the number of fishes feeding of habitatdestruction and mixingof gametesin best on benthicinvertebrates (e.g., darters).In the most availablespawning areas (Hubbs 1961,Greenfield et degradedsites, many IBI metricsreflect the serious al. 1973),and proportionof individuals with disease, degradationand reinforce the strength of the inference. tumors,fin damage, and major skeletal anomalies. The Finally,IBI metricshave differentialsensitivity along latterincreases in degradedareas, especially in areas thegradient from undisturbed to degraded(Fig. 3). withmajor toxic contamination (Brown et al. 1973, IBI scorescan be used to (1) evaluatecurrent con- Baumannet al. 1982).The anomalymetric uses only ditionsat a site,(2) determinetrends over time at a rapidsurvey procedures in searchof anomaliesthat site withrepeated sampling, (3) comparesites from can be discoveredby externalexamination without whichdata are collectedmore or less simultaneously, sacrificingfish. and (4) to someextent, identify the cause of local deg-

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 76 JAMES R. KARR Ecological Applications Vol. 1,No. 1 A B 45 - 0 Saline Branch a a Copper Slough 40 - o Kaskaskia Ditch 0 ~~~~~~~~~WWTP Tau= -733 cso Scioto River,Ohio - 35 P<.00l EWH

- - - - A ~~~~~~~~50 - ~~~ ~ ~ ) 30 A l~~~~~~~~~~~~ 98 7 WWH

25 - m 30 ' 20 20 ~~~~~~~~~~~~~~~~~~1979

0 0.5 1.0 1.5 2.0 210 200 190 180 170 Chlorine (mg/L) River Distance (km)

C D

100 Z excellent / / : Jordan 00 (n X XCreek a) 75 -: good 5.0 o> ILL c: 50 -fair >Oo 0

C) a 2 3.0 4 A~~~~~~~~~~0 j~25 poor 2 QBi 1.0 Ditch

0 25 50 75 30 40 50 60 % Urban Land Use IBI Total Score FIG. 4. (A) Indexof BioticIntegrity (IBI) as a functionof total residual chlorine content in threestreams in east-central Illinoiswith wastewater inflow from standard secondary treatment with chlorination (from Karr et al. 1985a). (B) Longitudinal trendin IBI forthe Scioto River, Ohio, in and downstreamfrom Columbus, Ohio, 1979and 1987.CSO = combinedsewer overflow;WWTP = wastewatertreatment plant inflow; WWH = warmwaterhabitat; EWH = excellentwarmwater habitat. Streamflow is fromleft to right(from Yoder 1989a, originallypublished with River Mile as horizontaldimension). (C) Contourplot of qualitative IBI ratingsas a functionof urbanization and % retentionof riparian forest (from Steedman 1988). (D) Standarddeviation of IBI valuesas a functionof IBI valuesin JordanCreek (0) and BigDitch (A), Illinois(from Karr etal. 1987). radation (Karr et al. 1986). Over 30 states and prov- spatialdynamics; (4) thereis no loss of information inces and several federalagencies have used IBI (or fromconstituent metrics when the total index is de- modificationsof IBI; see How to measurebiotic integ- terminedbecause each metriccontributes to thetotal rity:Adaptability of IBI, below). At least four states evaluation;and (5) professionaljudgment is incorpo- and the Tennessee Valley Authorityhave incorporated ratedin a systematicand ecologicallysound manner. IBI into their standards and monitoringprograms IBI does not serveall needs of detailedbiological (Miller et al. 1988), and many others are expanding monitoring(Karr et al. 1986,Fausch et al. 1990) and use of IBI and conceptuallysimilar approaches into certainlycannot be advocatedas a replacementfor theirroutine monitoring programs. physicaland chemicalmonitoring or toxicitytesting. Many advantagesof IBI have been cited(Karr 1981, However,ecologically sophisticated biological moni- Karr et al. 1986, Miller et al. 1988, Plafkinet al. 1989, toringprovides direct information about conditions at Fausch et al. 1990) including:(1) it is quantitative;(2) a samplesite comparedwith a sitewith little or no it gauges a stream against an expectationbased on humaninfluences or to theexpectation under a des- minimaldisturbance in theregion; (3) itreflects distinct ignatedbiological use classification(e.g., high-quality attributesof biologicalsystems, including temporal and warmwaterfishery).

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions February1991 BIOTIC INTEGRITY AND WATER RESOURCES 77 A sampling of successfuluses of IBI easilyobtained, especially from historical databases, Successfuluse ofIBI in a varietyof contexts (effects theprimary data available for initial development and of minedrainage, sewage effluent, habitat alteration, testingof IBI. For example,a sitewith johnny darter etc.)and in a diversityof geographicareas provethe (Etheostoma nigrum)and orange-throateddarter (E. utilityof theIBI concept(Karr et al. 1986,Miller et spectabile)is likelyto be degradedcompared with anal. 1988,Steedman 1988, Fausch et al. 1990,Oberdorff othersite withbanded (E. zonale) and slenderhead and Hughes,in press). darters(Percina phoxocephala). One approachto scor- Studieshave includedevaluation of chemicalfac- ingthese situations (Hughes and Gammon1987) is to tors,as illustratedby the inverse relationship between givea plus(+) to siteswith a preponderanceof species IBI and residualchlorine concentration in threewa- thatsuggest high quality. When IBI scoresare totaled, tershedsin east-centralIllinois (Karr et al. 1985a; see two or threespecies richness metrics with a plus ap- Fig. 4A). In anotherstudy, the effects of generalwa- pendedwould be scoredby addingone unitto IBI. tershedcondition and wastewatertreatment outflows Suchdifferences could be incorporatedinto future IBI wereevaluated in theScioto River, Ohio (Fig.4B). IBI applicationswhen relative rankings of severalspecies values werelow throughoutthe river in 1979, espe- as indicatorsof degradationare known.As another ciallydeclining below theinflow of wastewaterfrom example,one couldincorporate information on health largesewage treatment plants. After 8 yrof effortsto of individualfish through metrics such as condition controlthe plants' effluents, downstream biotic integ- factor(K) whereL is totallength (in millimetres)and rityimproved appreciably by 1987,although regional M is mass(in grams)K = (M/L3) x 105.Some effort nonpointsource and habitatdegradation keeps IBI be- mustbe madeto define a lengthclass for determination low optimallevels. ofK (Lagler1956). Alternatively, the age structureof In southernOntario, Steedman (1988) foundthat thepopulation might be used by examinationof the IBI wasstrongly associated with independently derived massesand/or lengths of individuals of selected species measuresof watershedcondition. He foundthat a or throughreading of growth annuli on scales.Use of thresholdof degradation for Toronto area streamswas eitherof these may improve the resolution of IBI eval- reachedunder conditions ranging from 75% removal uations,especially when applied to specificgroups of ofriparian vegetation in areaswith no urbanizationto sportfishspecies, or whensingle species dominate as- no (0%) removalof riparian vegetation at 55% urban- semblages(e.g., trout). ization.IBI ratingscould be expressedas a functionof Adaptationof IBI to geographicregions outside the proportionof basin in urbanland use (URB) and pro- midwesternUnited States requires modification, de- portionof order 1-3 channels with intact riparian forest letion,or replacementof selectedIBI metrics(Table (RIP) usingthe following equation: IBI = 30 - 19URB 2). Milleret al. (1988) providethe mostup-to-date + 14RIP.IBI hasalso beenused to showthat degraded reviewof changes needed to reflectregional differences sites(low IBI) are morevariable than less degraded in biologicalcommunities and fishdistribution. The sites(Fig. 4D). Further,between-stream differences in kind of flexibilityillustrated by IBI resultsfrom an IBI variabilitywere due to mobilityof fish and nearby integrativeframework with a strongecological foun- presenceof habitatrefuges (sources of colonists)in dation.Areas as diverseas the streamsof Colorado, JordanCreek (Karr et al. 1987), suggestingthat cu- New England,northern California, Oregon, southeast mulativeregional impacts may also be importantin Canada,France (Seine River), and Appalachiaand es- determininglocal bioticintegrity. tuariesin Louisiana,Chesapeake Bay, and New En- In short,IBI satisfiesthree conditions named by glandhave been evaluatedusing the conceptualap- Schindler(1987) foruseful monitoring programs: in- proachof IBI. expensive,simple, and highlysensitive to changesin In California,the principal attributes that must be ecosystems. accommodatedare reducedspecies richness, high en- demismamong watersheds, absence of midwestern taxa suchas dartersand sunfish,and highsalmonid abun- Adaptabilityof IBI dances.Modifications in IBI neededfor use in estuarine No singleindex or setof metrics can be expectedto areas of Louisianaincluded variation in salinityre- detectall waterresource problems. However, IBI is gimesand estuarysize. New IBI metricsreflect aspects verysuccessful as a broadlybased approachto assess of fishresidency, presence of nearshoremarine fishes thequality of a waterresource. IBI can be modifiedto and largefreshwater fishes, and a measureof seasonal incorporateother aspects of the fish community. Four variationin communitystructure. Other special con- suchaspects are (1) speciescomposition within major siderationsinclude the importance of streamgradient taxa,(2) populationstructure (e.g., size frequencydis- in Appalachiaand geographicvariation in tolerances tribution),(3) growthrates, and (4) relativehealth of of somespecies. For example,the creek chub (Semo- individualswithin populations of selected species. Karr tilusatromaculatus) varies appreciably in itstolerance (1981) mentionedall, but none were incorporated into of streamdegradation and foodhabits from Colorado theindex because the necessary information was not to Illinoisto theNew Riverdrainage of Virginia.

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 78 JAMES R. KARR Ecological Applications VA] 1 NA I Modificationsadopted by Ohio EPA includethe re- T = 0.546 placementof severalof theoriginal IBI metricswith 30 Pp<.001 alternatesfor analysis of conditions in large rivers. They propose replacementof darterswith round-bodied 03 * suckersin largerivers sampled with boat-mounted 0~~~~~~ .a_) 20 _ 40 electrofishinggear, an excellentsuggestion in a situa- ~~~4z^ tionwhere darters are likely to be undersampled.They 0 have,in addition,field tested and evaluatedother as- *- pectsof IBI. 10 _w *" Recentuse ofIBI bythe Tennessee Valley Authority 0 0 00 has shownits value in assessingdeclining biotic integ- 20 30 40 rity(Saylor and Scott1987, Wade and Stalcup1987). OriginolIBI In one case, releaseof cold waterlimited fish com- FIG. 5. Correlationbetween original IBI (Karr1981) and munitiesin a reservoirtailwater stream and in another modifiedIBI (Leonardand Orth1986) at sitesin WestVir- case low-flowperiods left much of the channel dry. In giniasampled by Leonard and Orth. bothcases, IBI detectedthis degradation when general reviewsof habitat conditions and water quality did not alertbiologists to problemsof waterresource degra- includelarge rivers in Oregon(Hughes and Gammon dation. 1987),Ohio (Ohio EPA 1988),and France(Oberdorff Perhapsthe most innovative use ofIBI is thework and Hughes,in press).Similar advances have been of Steedman(1988) in southernOntario. He sampled made in evaluationsof lakesin Minnesota(Heiskary fishesat 209 streamsites in 10 watershedsnear To- et al. 1987) and wetlands(Brooks and Hughes1988). ronto.All arein tributarieson thenorthwestern shore I attemptedwith limited success to applyIBI concepts of Lake Ontario.His 10-metricIBI includedseveral usingdata from a studyof birds of forest islands (Blake adaptationsto accommodateboth cold- and warm- 1983,Blake and Karr 1984, 1987). For example,the waterreaches, such as combiningtaxonomic groups in numberof omnivorous birds increases as forestisland selectedmetrics: sculpins plus darters, salmonids plus sizedeclines (Karr 1987). Apparently, the altered food centrarchids,and suckersplus catfishes. He foundthat basein remnantforest islands parallels changes in spe- within-yearvariation at samplesites on largerivers ciesrichness and abundance of omnivores in disturbed generallyfound IBI valueswithin ?4 points(4 out of headwaterstreams. 50 = 8%), and mostwere within ? 1 point.For between-yearcomparisons, >80% of samplesites had Assessmentof biotic integrity IBI valuesthat varied among years by < 10%. withother taxa Steedman'sanalysis of thresholdeffects in degra- The frameworkof the fish IBI has beenadopted by dationof riparianhabitat (Fig. 4C) raisesa persistent invertebratebiologists in effortsto develop robust but yetunanswered question about the thresholdof methodsto measuredegradation using benthic inver- riparianvegetation destruction within a watershedthat tebrate(Ohio EPA 1988,Plafkin 1989) and protozoan resultsin majordegradation of bioticintegrity (Karr communities(J. R. Pratt,unpublished manuscript). The and Schlosser1978). His approachusing IBI maypro- mostextensively tested, integrative effort is theInver- vide an indirectapproach to answeringthat question. tebrateCommunity Index (ICI) developedby Ohio It deservesconsiderable study in manygeographic ar- EPA (1988). ICI is a 10-metricindex (Table 4A) that eas. emphasizesstructural attributes of invertebratecom- Milleret al. (1988) encouragedmodification of IBI munities.Ohio EPA used this approachbecause of to make it suitablefor a wide rangeof geographical "acceptedhistorical use, simplederivation, and ease areas.Three cautions come to mind.First, avoid mod- ofinterpretation." Metric 10 is scoredbased on a qual- ificationsunless they yield significant improvement in itativefield sample, while metrics 1-9 are based on the utilityof theindex (Angermeier and Karr 1986). artificial-substratesampling. Forexample, Leonard and Orth (1986) modifiedmany As partof its effortto establishbiological metrics, IBI metricsfor study of streamsin WestVirginia. In USEPA hasalso supporteddevelopment of a hierarchy a reanalysisoftheir data, the ability ofthe IBI approach of methodsfor biological monitoring. Rapid Bioas- to detectdegradation was notimproved by their mod- sessmentProtocol III (Plaflinet al. 1989)is similarto ificationof metrics(Fig. 5). Second,modifications of the ICI but has onlyeight metrics (Table 4B). Both IBI shouldbe undertakenonly by experienced fish bi- structuraland functional metrics are included. RBP III ologistsfamiliar with the conceptual framework ofIBI, combinessampling invertebrates from a riffle/runhab- local fishfaunas, and watershedconditions. itatand froma grabsample of coarseparticulate or- Finally,efforts should be madeto developIBI-type ganicmatter (e.g., leaf packs) at each samplingsite. indexesfor use in other environments such as wetlands, Both effortsare promisingdevelopments designed lakes,and terrestrial ecosystems. Successful uses of IBI to strengthenthe role of biologyin assessmentof the

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TABLE 4. Metricsused to assessbiological integrity of ben- zation(population, community, ecosystem, and land- thicinvertebrate communities. scape). A. InvertebrateCommunity Index (ICI) (afterOhio EPA THEFUTURE OF BIOLOGICALMONITORING 1988*).Ratings of 6, 4, 2, and 0 are assignedto each metricaccording to whetherits value is comparableto Growingdissatisfaction with the adequacy of current exceptional,good, slightly deviates from a good,or strong- waterresource programs and recognitionof the poten- lydeviates from a goodcommunity. tial contributionof improvedbiological monitoring 1. Totalnumber of taxa 2. Totalnumber of mayfly taxa has stimulatednationwide interest in use ofbiological 3. Totalnumber of caddisfly taxa monitoringto attainthe goals of the Clean Water Act. 4. Totalnumber of dipteran taxa The needfor more rigorous use ofecological principles 5. Percentmayfly composition 6. Percentcaddisfly composition providesan unprecedentedopportunity for ecologists 7. PercentTribe Tanytarsini midge composition (biologists)to influence and even guide decisions about 8. Percentother dipteran and noninsectcomposition waterresources. How mightecologists contribute? 9. Percenttolerant organisms Biologyhas alwaysbeen a player(Ford 1989),but 10. Totalnumber of qualitative EPTt taxa nota principalplayer, in thewater resource arena. The B. Rapid BioassessmentProtocol III (afterPlafkin et al. 1989t).Ratings of 6, 3, and 0 aregiven based on values saprobicsystem (Kolkwitz and Marsson1908, 1909) of each of themetrics with 6 beinghigh quality and 0 was perhapsthe first major effort to use biologyin the beingheavily degraded site. assessmentof waterresource degradation. A classic 1. Taxonrichness paper(Patrick 1949) proved the importance of biolog- 2. Familybiotic index ical assessmentsto evaluationof the impacts of chem- 3. Ratioof scraper/filteringcollector 4. Ratioof EPTt and chironomidabundances icalpollutants. Cairns and his colleagues (Cairns 1974, 5. Percentcontribution of dominant family 1988a,b, Matthews et al. 1982)have built substantially 6. EPTt index on thatfoundation. Virtually all efforts,however, con- 7. Communityloss index 8. Ratioof shredders/total tinuethe focuson the evaluationof degradationde- rivingfrom chemical contamination (e.g., Worf 1980, * Metrics1-9 basedon artificialsubstrate sampler; metric 10 basedon qualitativestream sampling. Cairns1981). Duringthe past decadethe call forin- t EPT-taxa in theEmphemeroptera, Plecoptera, and Tri- creaseduse of biologicalassessment has been moti- choptera. vatedby the need to deal withchemical pollutants, t Metrics1-7 basedon qualitativeriffle/run sample; metric 8 basedon leaf-pack(CPOM) sample. bothpoint and nonpointsources, and theneed to re- verseother forms of water resource degradation (Karr and Dudley 1981,Karr 1987). The solutionof water qualityof water resources. The ICI is a robustaddition resourceproblems will not come from better regulation to the arsenalof assessmenttools. The RBP III has ofchemicals or thedevelopment of better assessment beenless extensively tested, and manyvalidation stud- toolsto detectdegradation caused by chemicals.The iesremain to be done.For example, the use of a random most criticalneed is to developmonitoring, assess- sampleof 100 invertebratesseems inadequate to me. ment,regulatory, and restoration approaches that eval- Invertebratecommunities often include 50 or more uatethe complex dynamics of degradation at locallev- species,making it unlikelythat a 100-individualsub- els and the cumulative regional impacts of samplewill be representativeof taxa and ecological anthropogenicdisturbance (Karr and Dudley 1981, groupsin such communities.Efforts are now being Bedfordand Preston1988). Rarely can environmental made to replacesome of the"ratio" metrics of RBP problemsbe tracedto "simplecauses, single distur- III withother metrics (M. T. Barbour,personal com- bances"(Bedford and Preston1988). munication).Other aspects of RBP III thatrequire more Manyindicators (Table 5) ofthe health of biological intensivetesting include its use overa widerrange of systemshave been testedin recentyears (National geographicareas, the adequacyof genusvs. species Academyof Sciences 1986, Schindler 1987, Taub 1987, levelidentifications, and theconstraint that sampling Ford 1989,Gray 1989, Levin et al. 1989,Pontasch et concentrateon onlya singlelocal habitat(riffle/run or al. 1989,Karr 1990). Each has sensitivityat different useof artificial substrates). These and other approaches levelsof degradation and to differentkinds of anthro- thatuse invertebrates (Berkman et al. 1986,Lenat 1988, pogenicstress. In addition,measurement difficulty var- J. R. Pratt,unpublished manuscript) in assessmentof iesconsiderably among them. The common occurrence bioticintegrity are not as widelyvalidated as is IBI, of severalbiological indicators among studies by so butthey show considerable promise as additionalwater manybiologists, however, suggest an unusualconsen- resourcetools. sus. Yet,the complexity of biological systems and the Fish and invertebrateIBI approachesare a major diversityof factors responsible for degradation, makes improvementover past programs in riverand stream itunlikely that any metric will have sufficient sensitiv- environments.Ecologists should strive to develop suites ityto be usefulunder all circumstances.As a result, ofmetrics that integrate taxa (fish,invertebrates, pro- biologistsare prone to rejectmany of the more specific tozoa, and diatoms)and levelsof ecologicalorgani- approachesthat show promise because they cannot be

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions 80 JAMES R. KARR Ecological Applications Vol. 1 No. 1 generalized. In fact,we should be integratingaspects TABLE 5. Biologicalindicators used to assesscondition of a of those promisingindicators to create a more robust waterresource with the goal of protectinghuman health, bioticintegrity, ora specificresource. An integrativeindex approach to biological monitoring. approachshould include representative metrics across a The success of IBI in a wide range of stream sizes rangeof these levels. and geographicareas comes fromits integrativeuse of the independent discoveries of many investigators. Bioassay-procedureof exposingtest organisms, in a labo- However,it is also not adequate. First,IBI was initially ratorysetting, to various concentrations ofsuspected toxicantsor dilutionsof whole effluent. restrictedto fish communities. Too much time and Singlespecies test energyhas been expended arguingabout which taxon Multispecies(microcosm, mesocosm) tests is most appropriate.I believe thatjust about any taxon Biosurvey-processof collectinga representativeportion of theorganisms living in thewater body of interest to could be selected and produce a reasonable level of determinethe characteristicsof the aquatic com- insightabout thewater resource if appropriate wisdom munity. is broughtto bear on developmentof robustand gen- Individual/speciespopulation (may involve selection of in- eral dicatorspecies) metrics. (Realistically, we must recognize that Tissueanalysis for bioaccumulation sampling,identification, or otherproblems might shift Biomarkers-geneticsor physiology the balance among taxa.) Use of the term IBI with Biomass/yield appropriatetaxonomic modifierscould help to reduce Growthrates Grossmorphology (external or internal) the tension(e.g., fishIBI, macroinvertebrateIBI). De- Behavior velopmentof suitesof metricsthat effectively integrate Abundance/density taxa mightalso be a goal. However, any use of the IBI Variationin populationsize Populationage structure concept should reflectthe use of a broadlybased array Disease or parasitismfrequency of metricsthat evaluate conditions fromindividual, Community/ecosystem(mayinvolve indicator taxa or guilds) population, community,and ecosystemlevels. Structure Several suggestionsare obvious. Speciesrichness/diversity First, ecologists Relativeabundances among species should supportefforts to incorporatebiology into the Tolerants/intolerants assessmentprocess. Second, ecologistsconducting en- Abundanceof opportunists vironmentalassessments must striveto overcome the Dominantspecies Communitytrophic structure tendencyto amass unorganizeddata. In manyrespects, Extinction theinability or reluctanceto distillthe biological mean- Function ing fromlarge quantities of data with rigorous,accu- Production/respirationratio rate,yet easily understood Production/biomassratio analyseshas diminishedthe Biogeochemicalcycles/nutrient leakage role of biology in waterresource management. Decomposition Finallyand most important,ecologists should make Landscape effortsto develop ways to apply advances in Habitatfragmentation/patch geometry ecological Linkagesamong patches theoryto the solutionof waterresource problems. The Cumulativeeffects across landscapes need forbiological input into evaluation of water resources is in many ways similarto the need thatstim- ulated the synthesis called conservation biology (Schonewald-Cox et al. 1983, Soule 1986, 1987). A respectto structureand functionin streamecosystems: core issue is how to use ecological knowledgeto im- river continuum (Vannote et al. 1980), patches and prove our abilityto measure and interpretthe effects boundaries(Schlosser 1982, Townsend 1989), and cli- of pollutantexposure or other human impacts on bi- matic variability(Schlosser 1987). Each draws atten- ological assemblages.We mustbe able to translatethis tion to specificattributes of streambiotas and the pat- knowledgeinto statementsabout the condition (eco- tern that they exhibit in space and time. The stream logical health)of these systems.Ecology as a discipline continuum hypothesisdepicts the stream as an up- must contendwith questions such as: (1) How can we stream-downstreamgradient of gradually changing optimize samplingdesign to detectpatterns given ex- physicalconditions and associated adjustmentsin en- istingspatial and temporalvariation? (2) How do we ergyprocesses and functionalattributes of the biota. identifyand defineimpairment? (3) How can we im- The food webs of headwater streamsare assumed to prove our abilityto detectinitial impairment (sensitive be primarilyallochthonous, while downstreamareas indicators,early warning indicators) as opposed to de- are more autochthonous.The trophicstructure of fish tectingonly massive degradation?(4) What should be and invertebratecommunities vary in concertwith food done to apply integrative,ecological approaches to resourceavailability. Some divergencefrom the stream monitoringin a wide diversityof biological systems? continuumpredictions have been documented (Win- Recent advances in understandingthe ecology of terbournet al. 1981). For example, the shiftfrom het- streams(see Matthewsand Heins 1987, Stanfordand erotrophyto autotrophychanges geographically (2nd- Covich 1988, Yount and Niemi 1990) should also 3rd orderstreams in the northwestvs. 4th or 5th order be used to improvethe conceptualfoundation and use in the northeast:Minshall et al. 1983). Cummins et al. of IBI. Three major world views are emergingwith (1989) provide a perceptivediscussion of the way the

This content downloaded from 128.173.125.76 on Wed, 12 Mar 2014 10:41:50 AM All use subject to JSTOR Terms and Conditions February1991 BIOTIC INTEGRITY AND WATER RESOURCES 81 streamcontinuum might be used to evaluateanthro- LITERATURE CITED pogeniceffects on streambiota. Angermeier,P. L., andJ. R. Karr. 1986. Applyingan index Accordingto the patches and boundariesidea, ofbiotic integrity based on stream-fishcommunities: con- streamsare complex landscapes (pools/riffles, small vs. siderationsin sampling and interpretation. North American Journalof Fisheries Management 6:418-429. largestreams, channel/wetland/upland transition) with Anonymous.1981a. WPCF roundtablediscussion-con- flowsacross the boundaries (Naiman et al. 1988)and gressionalstaffers take a retrospectivelook at PL 92-500. theregional pattern of patchesbeing of majorconse- Journalof the Water Pollution Control Federation 53:1264- quencein determiningthe attributes of specific streams. 1270. 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